The Impact of Nicotine along with Oral Contraceptive Exposure on Brain Fatty Acid Metabolism in Female Rats
Smoking-derived nicotine (N) and oral contraceptive (OC) synergistically exacerbate ischemic brain damage in females, and the underlying mechanisms remain elusive. In a previous study, we showed that N + OC exposure altered brain glucose metabolism in females. Since lipid metabolism complements glyc...
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Published in | International journal of molecular sciences Vol. 23; no. 24; p. 16075 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
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16.12.2022
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Abstract | Smoking-derived nicotine (N) and oral contraceptive (OC) synergistically exacerbate ischemic brain damage in females, and the underlying mechanisms remain elusive. In a previous study, we showed that N + OC exposure altered brain glucose metabolism in females. Since lipid metabolism complements glycolysis, the current study aims to examine the metabolic fingerprint of fatty acids in the brain of female rats exposed to N+/-OC. Adolescent and adult Sprague-Dawley female rats were randomly (n = 8 per group) exposed to either saline or N (4.5 mg/kg) +/-OC (combined OC or placebo delivered via oral gavage) for 16-21 days. Following exposure, brain tissue was harvested for unbiased metabolomic analysis (performed by Metabolon Inc., Morrisville, NC, USA) and the metabolomic profile changes were complemented with Western blot analysis of key enzymes in the lipid pathway. Metabolomic data showed significant accumulation of fatty acids and phosphatidylcholine (PC) metabolites in the brain. Adolescent, more so than adult females, exposed to N + OC showed significant increases in carnitine-conjugated fatty acid metabolites compared to saline control animals. These changes in fatty acyl carnitines were accompanied by an increase in a subset of free fatty acids, suggesting elevated fatty acid β-oxidation in the mitochondria to meet energy demand. In support, β-hydroxybutyrate was significantly lower in N + OC exposure groups in adolescent animals, implying a complete shunting of acetyl CoA for energy production via the TCA cycle. The reported changes in fatty acids and PC metabolism due to N + OC could inhibit post-translational palmitoylation of membrane proteins and synaptic vesicle formation, respectively, thus exacerbating ischemic brain damage in female rats. |
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AbstractList | Smoking-derived nicotine (N) and oral contraceptive (OC) synergistically exacerbate ischemic brain damage in females, and the underlying mechanisms remain elusive. In a previous study, we showed that N + OC exposure altered brain glucose metabolism in females. Since lipid metabolism complements glycolysis, the current study aims to examine the metabolic fingerprint of fatty acids in the brain of female rats exposed to N+/−OC. Adolescent and adult Sprague–Dawley female rats were randomly (n = 8 per group) exposed to either saline or N (4.5 mg/kg) +/−OC (combined OC or placebo delivered via oral gavage) for 16–21 days. Following exposure, brain tissue was harvested for unbiased metabolomic analysis (performed by Metabolon Inc., Morrisville, NC, USA) and the metabolomic profile changes were complemented with Western blot analysis of key enzymes in the lipid pathway. Metabolomic data showed significant accumulation of fatty acids and phosphatidylcholine (PC) metabolites in the brain. Adolescent, more so than adult females, exposed to N + OC showed significant increases in carnitine-conjugated fatty acid metabolites compared to saline control animals. These changes in fatty acyl carnitines were accompanied by an increase in a subset of free fatty acids, suggesting elevated fatty acid β-oxidation in the mitochondria to meet energy demand. In support, β-hydroxybutyrate was significantly lower in N + OC exposure groups in adolescent animals, implying a complete shunting of acetyl CoA for energy production via the TCA cycle. The reported changes in fatty acids and PC metabolism due to N + OC could inhibit post-translational palmitoylation of membrane proteins and synaptic vesicle formation, respectively, thus exacerbating ischemic brain damage in female rats. Smoking-derived nicotine (N) and oral contraceptive (OC) synergistically exacerbate ischemic brain damage in females, and the underlying mechanisms remain elusive. In a previous study, we showed that N + OC exposure altered brain glucose metabolism in females. Since lipid metabolism complements glycolysis, the current study aims to examine the metabolic fingerprint of fatty acids in the brain of female rats exposed to N+/-OC. Adolescent and adult Sprague-Dawley female rats were randomly (n = 8 per group) exposed to either saline or N (4.5 mg/kg) +/-OC (combined OC or placebo delivered via oral gavage) for 16-21 days. Following exposure, brain tissue was harvested for unbiased metabolomic analysis (performed by Metabolon Inc., Morrisville, NC, USA) and the metabolomic profile changes were complemented with Western blot analysis of key enzymes in the lipid pathway. Metabolomic data showed significant accumulation of fatty acids and phosphatidylcholine (PC) metabolites in the brain. Adolescent, more so than adult females, exposed to N + OC showed significant increases in carnitine-conjugated fatty acid metabolites compared to saline control animals. These changes in fatty acyl carnitines were accompanied by an increase in a subset of free fatty acids, suggesting elevated fatty acid β-oxidation in the mitochondria to meet energy demand. In support, β-hydroxybutyrate was significantly lower in N + OC exposure groups in adolescent animals, implying a complete shunting of acetyl CoA for energy production via the TCA cycle. The reported changes in fatty acids and PC metabolism due to N + OC could inhibit post-translational palmitoylation of membrane proteins and synaptic vesicle formation, respectively, thus exacerbating ischemic brain damage in female rats. |
Author | Perez-Pinzon, Miguel A Patel, Shahil H Dave, Kunjan R Mankaliye, Berk Timón-Gómez, Alba Raval, Ami P Pradhyumnan, Hari |
AuthorAffiliation | 2 Department of Neurology, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA 1 Peritz Scheinberg Cerebral Vascular Disease Research Laboratories, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA 4 Bruce W. Carter Department of Veterans Affairs Medical Center, Miami, FL 33136, USA 3 Neuroscience Program, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA |
AuthorAffiliation_xml | – name: 2 Department of Neurology, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA – name: 4 Bruce W. Carter Department of Veterans Affairs Medical Center, Miami, FL 33136, USA – name: 3 Neuroscience Program, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA – name: 1 Peritz Scheinberg Cerebral Vascular Disease Research Laboratories, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA |
Author_xml | – sequence: 1 givenname: Shahil H surname: Patel fullname: Patel, Shahil H organization: Department of Neurology, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA – sequence: 2 givenname: Alba orcidid: 0000-0001-9811-8557 surname: Timón-Gómez fullname: Timón-Gómez, Alba organization: Department of Neurology, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA – sequence: 3 givenname: Hari surname: Pradhyumnan fullname: Pradhyumnan, Hari organization: Department of Neurology, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA – sequence: 4 givenname: Berk surname: Mankaliye fullname: Mankaliye, Berk organization: Department of Neurology, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA – sequence: 5 givenname: Kunjan R surname: Dave fullname: Dave, Kunjan R organization: Neuroscience Program, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA – sequence: 6 givenname: Miguel A surname: Perez-Pinzon fullname: Perez-Pinzon, Miguel A organization: Neuroscience Program, Leonard M. Miller School of Medicine, University of Miami, Miami, FL 33136, USA – sequence: 7 givenname: Ami P orcidid: 0000-0003-1757-9947 surname: Raval fullname: Raval, Ami P organization: Bruce W. Carter Department of Veterans Affairs Medical Center, Miami, FL 33136, USA |
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Keywords | nicotine metabolomics phosphatidylcholine β-oxidation carnitine palmitoyltransferase enzymes 1 and 2 phospholipids stroke oral contraceptive palmitoylation |
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SubjectTerms | Age Animals Brain Brain - metabolism Brain damage Brain injury Carnitine carnitine palmitoyltransferase enzymes 1 and 2 Chromatography Contraceptives Contraceptives, Oral Cytochrome Enzymes Experiments Exposure Fatty acids Fatty Acids - metabolism Female Females Glucose metabolism Glycolysis Hormone replacement therapy Humans Ischemia Kinases Laboratory animals Lecithin Lipid Metabolism Lipids Membrane proteins Metabolism Metabolites Metabolomics Mitochondria Nicotine oral contraceptive Oral contraceptives Oxidation Oxidation-Reduction Palmitoylation Phosphatidylcholine phospholipids Post-translation Proteins Rats Rats, Sprague-Dawley Software Tricarboxylic acid cycle β-oxidation |
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Title | The Impact of Nicotine along with Oral Contraceptive Exposure on Brain Fatty Acid Metabolism in Female Rats |
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